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Insight Into the Hidden Bacterial Diversity of Lake Balaton, Hungary

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Insight Into the Hidden Bacterial Diversity of Lake Balaton, Hungary Biologia Futura (2020) 71:383–391 https://doi.org/10.1007/s42977-020-00040-6 ORIGINAL PAPER Insight into the hidden bacterial diversity of Lake Balaton, Hungary E. Tóth1 · M. Toumi1 · R. Farkas1 · K. Takáts1 · Cs. Somodi1 · É. Ács2,3 Received: 22 May 2020 / Accepted: 17 August 2020 / Published online: 7 September 2020 © The Author(s) 2020 Abstract In the present study, the prokaryotic community structure of the water of Lake Balaton was investigated at the littoral region of three diferent points (Tihany, Balatonmáriafürdő and Keszthely) by cultivation independent methods [next-generation sequencing (NGS), specifc PCRs and microscopy cell counting] to check the hidden microbial diversity of the lake. The taxon-specifc PCRs did not show pathogenic bacteria but at Keszthely and Máriafürdő sites extended spectrum beta- lactamase-producing microorganisms could be detected. The bacterial as well as archaeal diversity of the water was high even when many taxa are still uncultivable. Based on NGS, the bacterial communities were dominated by Proteobacteria, Bacteroidetes and Actinobacteria, while the most frequent Archaea belonged to Woesearchaeia (Nanoarchaeota). The ratio of the detected taxa difered among the samples. Three diferent types of phototrophic groups appeared: Cyanobacteria (oxy- genic phototrophic organisms), Chlorofexi (anaerobic, organotrophic bacteria) and the aerobic, anoxic photoheterotrophic group (AAPs). Members of Firmicutes appeared only with low abundance, and Enterobacteriales (order within Proteobac- teria) were present also only in low numbers in all samples. Keywords Lake Balaton · Bacterial diversity · Archaea · Bacteria · Next-generation sequencing (NGS) Introduction (Istvánovics et al. 2008; Bolla et al. 2010; Hatvani et al. 2014; Maasz et al. 2019). Lake Balaton is the biggest lake of Central Europe, a shal- The frst microbiological investigations aimed at studying low water ditch, with an average depth of 3.0–3.6 m. The the prokaryotic diversity of the lake showed that members open water of the lake is almost permanently homogenized of the genus Bacillus (Firmicutes) are dominant at some by wind, resulting concomitant resuspension of the sedi- regions (Langó 1982). Diferent Actinobacteria were also ment. The lake has a great importance also due to its tour- isolated from the water of Keszthely Bay, e.g. Streptomy- istical use. The quality of the water is regularly tested, and ces and Micromonospora species (Farkas 1982). In 1985, monitoring has started already in the 1960s (Szabó 1999; the presence of Enterobacteria (indicating faecal pollution) Kiss et al. 2005). In 2006, Hungary joined the water quality was found in Keszthely Bay, and Enterobacter agglomer- assessments in line with the EU Water Framework Direc- ans, Escherichia coli, Kluyvera cryocrescens and Klebsiella tive (EU WFD). In it, the defnitions of biological variables oxytoca were detected in high number among the cultivated were given a much stronger role than before. Moreover, till bacterial strains (Bognár, 1990). that time many studies had revealed the state of the water Tóth (1995) has studied the bacterial communities of the open water in the Balatonfüred region and found the domi- nance of many Gram-negative organisms belonging to the genera Aeromonas, Pseudomonas and Acinetobacter. Bacte- * E. Tóth rial partners of Eudiaptomus gracilis (important member of [email protected] the zooplankton of the lake) were also studied (Homonnay 1 Department of Microbiology, Eötvös Loránd University, et al. 2011) as well as the microbiology of big-headed carps Budapest, Hungary (Borsodi et al. 2017). The frst detailed reports about aerobic 2 MTA Centre for Ecological Research, Danube Research anoxygenic phototrophs (AAPs) of the lake showed that their Institute, Budapest, Hungary abundance as compared to heterotrophic bacteria is between 3 National University of Public Service, Faculty of Water 1 and 7% (Szabó-Tugyi et al. 2019). Sciences, Baja, Hungary Vol.:(0123456789)1 3 384 Biologia Futura (2020) 71:383–391 All of these studies are very important, but most of them DNA extraction from the water samples were based on cultivation techniques, and it is known that less than 1% of bacteria are cultivable from natural aquatic For DNA extraction, 0.25L water samples were fil- habitats (Amann et al. 1995). tered through 0.22 μm pore size, mixed cellulose fil- The aim of the present study was to reveal the prokaryotic ter (type GSWP; Millipore, Billerica, MA, USA) using community structure of the water of the lake at the littoral the Ultraclean® PowerSoil DNA Isolation Kit (MoBio, region (where the water is subjected also to strong human Carlsbad, CA, USA) according to the manufacturer’s infuence due to bathing) by cultivation independent meth- instructions. ods [next-generation sequencing (NGS) and microscopic cell counting]. By using specifc PCRs, the presence of some hygienically important bacteria was tested. Our results show Specifc PCRs the hidden prokaryotic diversity of the lake which has never been revealed until now, and provide information about the Taxon-specifc PCRs were applied for the following bacte- potential health risks of bathing. rial groups: Pseudomonas spp. and Pseudomonas aerugi- nosa according to Lavenir et al. (2007), Legionella spp. according to Cloud et al. (2000), Legionella pneumophila Materials and methods according to Fiume et al. (2005), Acinetobacter baumannii according to Tsai et al. (2018) and Stenotrophomonas malt- Sampling ophilia according to Filho et al. (2004). At the sampling sites there were no people at the time of Sampling was carried out in 30. 08. 2018 at three points sampling (it was late pm), but the sites were subjected to of the lake: Tihany (65.91900 N; 17.88903 E), Kesz- bathing in the previous days, therefore, the bacterial com- thely (46.76014 N; 17.25448 E) and Balatonmáriafürdő munity was tested also for extended spectrum beta-lactamase (46.70725 N; 17.38276 E) (later: Máriafürdő), from the lit- (ESBL)-producing and macrolide-resistant bacteria. toral water region. The water samples (1–1 L) were asep- The presence of ESBL genes was tested by multiplex tically collected into sterilized screw-capped fasks from PCRs in the water samples according to Trung et al. (2015) 10 cm subsurface according to ISO 19458:2006. Samples and macrolide-resistance genes following the protocol were transported to the laboratory in a cooler bag (at 4 °C) described by Zmantar et al. (2011), testing fve genes (ermA, and processed within 4 h after sampling. ermB, ermC, msrA and mefA) simultaneously. Analysis of physical and chemical parameters Next‑generation DNA sequencing and data analysis To measure the physical and chemical parameters, the fol- For the identifcation of bacterial and archaeal taxa, the 16S lowing standards were used: MSZ 448-32:1977 (conductiv- rRNA gene of the DNA samples was amplifed with PCRs ity), MSZ ISO 5813:1992 (dissolved oxygen, DOC), MSZ in separate, triplicate reactions using primers with the fol- 1484-13:2009 (nitrate concentration), MSZ 448-13-1983 lowing target-specifc sequences: Bact_341F (5′-CCT ACG (sulphate concentration), MSZ ISO 10260:1993 (chlorophyll GGN GGC WGC AG-3′) and modifed Bact_805R (5′-GAC a). The measures were done by the Central Transdanubian TAC NVG GGT ATC TAA TCC-3′) for bacteria (Herlemann Water Authority, and we got it via the National Directorate et al. 2011), and A519F (5′ -CAG CMG CCG CGG TAA- of Water Management (OVF); data were obtained from the 3′) and Arch855R (5′ -TCC CCC GCC AAT TCC TTT ofce except values of water temperature and pH which were AA-3′) for Archaea (Klindworth et al. 2013). DNA sequenc- measured on site. ing was performed on an Illumina MiSeq platform using MiSeq standard v2 chemistry by the Genomics Core Facil- Determination of microscopy cell counts ity RTSF, Michigan State University, USA. Sequencing and the description of bioinformatic analysis were done accord- Determination of bacterioplankton abundance (micros- ing to Benedek et al. (2019). OTUs were determined at the copy cell counts) was carried out as described by Kéki species-level delineation based on Tindall et al. (2010). et al. (2019) using Nikon80i epifuorescent microscopy Sequence reads were deposited in the NCBI SRA database and NisElements program package. For the investigations, and are accessible through the BioProject PRJNA628507, 10 mL water samples were fltered on sterile polycarbonate Biosample ID SAMN14732963 (Tihany), SAMN14732959 flters (Millipore, Billerica, MA, USA) and fxed with 2% (Máriafürdő) and SAMN14732964 (Keszthely). Diversity paraformaldehyde solution. indices were calculated using mothur (Schloss et al. 2009), 1 3 Biologia Futura (2020) 71:383–391 385 and reads were subsampled to the read number of the sample having the lowest sequence count. Cell count/mL 6.34E+06 6.13E+06 Results 2.75E+06 Physico‑chemical and biological parameters (mg/l 2− 4 94 91 119 The physico-chemical parameters together with the cell SO count values of the samples of the Lake Balaton are given in Table 1. Data of the three sampling sites showed similari- (mg/l) − ties though some diferences could be detected: the quantity 3 0.1 0.1 0.1 of total organic carbon (TOC), total organic nitrogen (TON), NO total organic phosphorous (TOP) as well as chlorophyll-a ) concentration were the lowest in the Tihany region. Most 3 TOC appeared in dissolved form (DOC), and the water was 5.33 aerated at all sites. 7.7 21.3 Chlorophyll Chlorophyll a (mg/m Specifc PCRs The taxon-specific PCRs showed (Table 2) that Pseu- 39 66 65 domonas spp. and Legionella spp. were present at all sites, (μg/L) TOP but pathogenic L. pneumophila and P. aeruginosa as well as Acinetobacter baumannii could not be detected. At Kes- zthely and Máriafürdő sites ESBL-producing bacteria could 0.646 0.956 0.766 also be detected. (mg/L) TON Amplicon sequencing NGS results showed that diversity indices of Keszthely 7.6 8.5 8.7 and Máriafürdő samples were similar in case of all types DOC (mg/L) of indices, while Tihany sample (despite the fact that cell counts were high even at that site) produced much lower values.
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